Shafer LA, Biraro S, Nakiyingi-Miiro J, et al. HIV prevalence and incidence are no longer falling in southwest Uganda: evidence from a rural population cohort 1989-2005. AIDS 2008;22(13):1641-9.
To examine trends in HIV prevalence, incidence, and sexual behavior in a rural population cohort in Uganda over 16 years (1989 to 2005)
A 16-year annual census of the population of rural villages in southwest Uganda, beginning with 15 villages in 1989 and adding 10 in 1999. Survey rounds began in November and ended in October of the next year. After obtaining consent, survey staff administered risk factor questionnaires to individuals, after which blood was taken for HIV-1 tests. Interviewers obtained census data through annual household visits.
25 villages in a rural area of southwest Uganda
An average of 6279 adults (aged 13 years or older) was included in the census each year in survey rounds 1-10. In survey rounds 11-16, after 10 villages were added to the cohort, an average of 11,139 adults was included in the census each year. Across all 16 rounds, 75.8% of included adults had confirmed HIV-status results in the rounds in which they were included. For the analysis of incidence, data were collected from 14,449 individuals who were uninfected with HIV at first test and who had two or more tests.
There was no intervention.
The first primary outcome was HIV prevalence by survey round. Individual HIV status was determined as follows: in a given round, if an individual was tested for HIV, the result was used. If the individual could not be tested and had been classified as seropositive during a previous round, it was assumed that this person was infected with HIV. Similarly, if an individual was classified as seronegative in a subsequent survey round, it was assumed that the individual was not infected with HIV. Prevalence was the proportion of the population residents during the survey round known to be HIV infected. The second primary outcome was HIV incidence by calendar year. The mid-date between the last negative and first positive HIV test result was estimated as the date of seroconversion. In incidence analyses, all time up to the last HIV test if uninfected, or estimated date of seroincidence if an HIV seroconversion occurred, was included in calculating the person-years at risk (PYAR). This includes time in which the person may have temporarily moved their residence away from the catchment area, as long as the individual returned to the area and received at least one HIV test after doing so. The third primary outcome was indicators of sexual behavior. Indicators including casual partners, condom use, pregnancies, and age at sexual debut were measured through interviewer-administered risk factor questionnaires.
Prevalence of HIV-1 declined from 8.5% in 1990/1991 to 6.2% in 1999/2000 and thereafter rose to 7.7% in 2004/2005. Women had higher prevalence than men in all rounds, but the trend did not differ between men and women. Incidence (per 1000 PYAR) fell from 7.5 in 1990 to 4.1 in 1998 and thereafter increased to 5.0 by 2004. The 2005 incidence estimate reached an all-time low of 2.5, but the preliminary 2006 estimate rose. Incidence patterns varied by age and sex, although both men and women experienced a downward trend in incidence followed by an increase until 2004. Trends and patterns among different age groups were not statistically significant. Some sexual behavior indicators showed more risky behavior in recent years compared with the 1990s, whereas others showed that this reduction continues. Among all age groups, except that of people aged 13-19 years, the percentage claiming to have had one or more casual partners rose between 1997 and 2004. There was a reduction in 2005, but the older age groups still showed a larger percentage than in 1997. The only trend that reached statistical significance was that among the age group of people aged 35-44 years (P=0.003). This result coincides both with stabilized incidence in the whole adult population from 1998 to 2004 and with the increasing incidence of HIV in men aged 35 years or older. By contrast, among the youngest age group (aged 13-19 years), the trend towards fewer participants claiming to have had one or more casual partners in the last year was nearly significant (P=0.069). Among youth aged 20-24 years, condom use with casual partners dropped from 74.1% in 1997 to 50.7% in 2005 (P=0.057). By contrast, among those aged 45 years or older, condom use with casual partners increased from 10.0% in 1997 to 24.4% in 2005 (P=0.071).
The percentage of never-married adolescent women (aged 15-19 years) who have ever been pregnant fell rapidly throughout the 1990s to 1998, but since then, this decreasing trend has stopped (P=0.034). For both sexes, the median age at sexual debut as reported by 16-19-year-olds rose steadily between 1997, the first year in which the age at first sex was asked, and 2005. In most years from 1993 onwards, information also was collected on whether young people had ever had sex. Among young men, there is a pattern that holds true for each age (15- through 18-year-olds) separately. That is, among these young men, the percentage of individuals who have ever had sex declined between 1993 and 1997, but increased between 1998 and approximately 2000. Finally, from 2002 onward, the percentage is slightly lower than it is between 1993 and 1997 and is generally stable. This interesting pattern among young men displays a temporary increase in the percentage that have ever had sex, which coincides with the time period during which overall incidence in the population showed a rising trend and incidence among young men also had a temporary increase. Among young women, a similar temporary increase in the percentage that have ever had sex occurred between 1997 and 2000, but this was observed in two age groups only.
The authors conclude that HIV-1 prevalence is rising in this cohort and that incidence is stabilizing and showing signs of increasing among some subgroups. The extent to which changing sexual behavior has played a role in these epidemiological trends is unclear, but it is likely to have contributed.
Although the authors describe this study as a cohort, individuals were not followed from baseline and no account of the annual number and characteristics of residents leaving or moving into the villages was provided. As an example, 14,449 individuals contributed to the incidence analysis, but the total number that might have contributed is not provided and the effect of possible migration and emigration is not discussed. Therefore, it seems inappropriate to attempt to rate this as a cohort study. As a series of population censuses, it appears to be of relatively high quality, but the impact of annual changes in the population on the estimates of prevalence and incidence is difficult to assess. Because eligible persons began receiving ART in the beginning of 2004, (7.5% of HIV-infected residents in this cohort in 2004 and 15.6% in 2005), it is likely that the round 16 (2005) estimate of prevalence was partially influenced by reduced mortality due to ART, but it is unlikely that any of the earlier rounds were influenced. There was no change in the proportion of resident individuals who agreed to an HIV test since 2004, so it is unlikely that sick people were more likely to agree to testing as a result of the availability of ART. Because the estimation method uses data from previous and subsequent rounds, estimated prevalence from the first survey is biased downward and the most recent estimate is provisional. The rate of age-standardized mortality among adults who were included in the census but who did not have blood samples taken was higher than the combined mortality rate among HIV-infected and HIV-uninfected participants. This result could have been due to a higher rate of HIV infection among those who did not participate in the serosurvey and rapid progression to death. This bias may have influenced estimated trends, as the percentage of people who agreed to an HIV test has decreased in recent years. If anything, however, the bias would make the estimate of a rising trend in HIV prevalence conservative. Incidence estimates are likely to be slightly biased downward because some people who progressed rapidly through stages of HIV may have become infected and died before their infection could have been detected by annual HIV testing.
Uganda was one of the first African countries to report cases of HIV infection. By 1989, when large-scale tracking of the epidemic, including the establishment of two population cohorts, had begun, the HIV epidemic had already reached a generalized level. Largely due to the early response initiated by the Ugandan government,(1) Uganda was among the first countries to achieve a decline in HIV prevalence. Throughout the 1990s, HIV prevalence and incidence fell in Uganda, and this was attributed primarily to reductions in risky sexual behavior.(2) Neighboring countries, as well as the international community at large, have looked to Uganda as a model of effective control of the epidemic. Recently, some researchers noticed that HIV-1 prevalence seems to be leveling off.(1) Until now, however, this evidence has been scanty and has been based on trends in HIV prevalence seen in antenatal clinics (ANCs) and voluntary counseling and testing (VCT) sites. Much research has warned against relying solely on prevalence data to support conclusions about a changing epidemic.(3)
To solidify the success that Uganda had throughout the 1990s in controlling the HIV epidemic, efforts in HIV prevention must be re-strengthened using all strategies known. Because the evidence of changing sexual behavior in recent years is ambiguous, it is critical to study sexual behavior in greater detail. If sexual behavior is becoming more risky in this population, an exploration of the reasons for this change is paramount to advise public health policy. This study also points to the need to track and address the changing HIV epidemic in other countries through incidence estimates rather than prevalence estimates alone.
- MOH-Uganda. Uganda HIV/AIDS sero-behavioural survey 2004-2005. Calverton, Maryland, USA: Ministry of Health (Uganda) and ORC Macro; 2006. Abstract not available.
- Kamali A, Carpenter L, Whitworth J, Pool R, Ruberantwari A, Ojwiya A. Seven-year trends in HIV-1 infection rates, and changes in sexual behaviour among adults in rural Uganda. AIDS 2000;14:427-34.
- Wawer MJ, Serwadda D, Gray RH, et al. Trends in HIV-1 prevalence may not reflect trends in incidence in mature epidemics: data from the Rakai population-based cohort, Uganda. AIDS 1997;11:1023-30.